Isotopic tracing reveals single-cell assimilation of a macroalgal polysaccharide by a few marine Flavobacteria and Gammaproteobacteria

• Published in: The ISME Journal Vol. 15; no. 10; pp. 3062 - 3075
• Main Authors: Thomas, François, Le Duff, Nolwen, Wu, Ting-Di, Cébron, Aurélie, Uroz, Stéphane, Riera, Pascal, Leroux, Cédric, Tanguy, Gwenn, Legeay, Erwan, Guerquin-Kern, Jean-Luc
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 01.10.2021; Nature Publishing Group
• Subjects: 13/31; 14/32; 45/22; 45/23; 631/326/171/1878; 631/326/2565/855; 631/326/41/2535; 631/326/47; 704/158/855; Algae; Alginates; Alginic acid; Alteromonadales; Assimilation; Bacteria; Bacteriology; Biodegradation; Biomedical and Life Sciences; Carbon; Carbon 13; Carbon cycle; Coastal ecology; Coastal ecosystems; Deoxyribonucleic acid; DNA; Earth Sciences; Ecology; Evolutionary Biology; Flavobacteriaceae; Flavobacterium; Gammaproteobacteria; Gammaproteobacteria - genetics; Heterotrophic bacteria; Hybridization; Isotopic tracers; Life Sciences; Mass spectrometry; Mass spectroscopy; Metagenomics; Microbial activity; Microbial Ecology; Microbial Genetics and Genomics; Microbiology; Microbiology and Parasitology; Microbiota; Microorganisms; Oceanography; Organic matter; Polysaccharides; Saccharides; Sciences of the Universe; Seaweeds; Secondary ion mass spectrometry; Stable isotopes; Substrates; Microbial ecology; Water microbiology; Biogeochemistry; Marine microbiology
• ISSN: 1751-7362; 1751-7370
• DOI: 10.1038/s41396-021-00987-x

Algal polysaccharides constitute a diverse and abundant reservoir of organic matter for marine heterotrophic bacteria, central to the oceanic carbon cycle. We investigated the uptake of alginate, a major brown macroalgal polysaccharide, by microbial communities from kelp-dominated coastal habitats. Congruent with cell growth and rapid substrate utilization, alginate amendments induced a decrease in bacterial diversity and a marked compositional shift towards copiotrophic bacteria. We traced 13 C derived from alginate into specific bacterial incorporators and quantified the uptake activity at the single-cell level, using halogen in situ hybridization coupled to nanoscale secondary ion mass spectrometry (HISH-SIMS) and DNA stable isotope probing (DNA-SIP). Cell-specific alginate uptake was observed for Gammaproteobacteria and Flavobacteriales , with carbon assimilation rates ranging from 0.14 to 27.50 fg C µm −3 h −1 . DNA-SIP revealed that only a few initially rare Flavobacteriaceae and Alteromonadales taxa incorporated 13 C from alginate into their biomass, accounting for most of the carbon assimilation based on bulk isotopic measurements. Functional screening of metagenomic libraries gave insights into the genes of alginolytic Alteromonadales active in situ. These results highlight the high degree of niche specialization in heterotrophic communities and help constraining the quantitative role of polysaccharide-degrading bacteria in coastal ecosystems.